Stimulation of zero-trans rates of lactose and maltose uptake into yeasts by preincubation with hexose to increase the adenylate energy charge

Applied and Environmental Microbiology

Volumn 74, Issue 10, 2008, Pages 3076-3084

  Guimarães, Pedro M R ^a,b   Multanen, Jyri Pekka ^a   Domingues, Lucília ^b   Teixeira, José A ^b   Londesborough, John ^a  

^a VTT TECHNICAL RESEARCH CENTRE OF FINLAND   (Finland)

^b UNIVERSITY OF MINHO   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

FERMENTATION; GROWTH KINETICS; NUTRIENTS; YEAST;

ADENYLATE ENERGY CHARGE; METABOLIZING CELLS;

MALTOSE;

ADENOSINE PHOSPHATE; BETA GALACTOSIDASE; CARBON 14; HEXOSE; LACTOSE; MALTOSE; PROTON; ADENOSINE TRIPHOSPHATE; BETA FRUCTOFURANOSIDASE; CARBON; COTRANSPORTER; GLUCOSE; GLUCOSE 6 PHOSPHATE ISOMERASE;

BIOASSAY; ELECTROCHEMISTRY; ENZYME ACTIVITY; FERMENTATION; METABOLISM; RADIOACTIVITY; RECOMBINATION; SUGAR; YEAST;

ARTICLE; CELL METABOLISM; ENERGY; ENZYME ACTIVITY; FERMENTATION; GLUCOSE TRANSPORT; KLUYVEROMYCES; NONHUMAN; SACCHAROMYCES CEREVISIAE; YEAST; CHEMISTRY; CYTOPLASM; METABOLISM;

KLUYVEROMYCES LACTIS; SACCHAROMYCES CEREVISIAE;

ADENOSINE TRIPHOSPHATE; BETA-FRUCTOFURANOSIDASE; BETA-GALACTOSIDASE; CARBON RADIOISOTOPES; CYTOPLASM; GLUCOSE; GLUCOSE-6-PHOSPHATE ISOMERASE; KLUYVEROMYCES; LACTOSE; MALTOSE; PERIPLASM; SACCHAROMYCES CEREVISIAE; SYMPORTERS;

EID: 44249113845     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.00188-08     Document Type: Article

References (50)

1. Alves-Araújo, C., A. Pacheco, M. J. Almeida, I. Spencer-Martins, C. Leão, and M. J. Sousa. 2007. Sugar utilization patterns and respiro-fermentative metabolism in the baker's yeast Torulaspora delbrueckii. Microbiology 153:898-904.
2. +-ATPase. J. Exp. Biol. 203:155-160.
3. Ball, W. J., and D. E. Atkinson. 1975. Adenylate energy charge in Saccharomyces cerevisiae during starvation. J. Bacteriol. 121:975-982.
4. Barnett, J. A., and A. P. Sims. 1982. The requirement of oxygen for the active transport of sugars into yeasts. J. Gen. Microbiol. 128:2303-2312.
5. Bissen, L. F., and D. G. Fraenkel. 1983. Involvement of kinases in glucose and fructose uptake by Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 80:1730-1734.
6. Boze, H., G. Moulin, and P. Galzy. Galactose and lactose transport in Kluyveromyces lactis. Folia Microbiol. 32:107-111.
7. Carvalho-Silva, M., and I. Spencer-Martins. 1990. Modes of lactose uptake in the yeast species Kluyveromyces marxianus. Antonie van Leeuwenhoek 57:77-81.
8. Dickson, R. C., L. R. Dickson, and J. S. Markin. 1979. Purification and properties of an inducible β-galactosidase isolated from the yeast Kluyveromyces lactis. J. Bacteriol. 137:51-61.
9. Dickson, R. C., and K. Barr. 1983. Characterization of lactose transport in Kluyveromyces lactis. J. Bacteriol. 154:1245-1251.
10. Diderich, J. A., M. Schepper, P. van Hoek, M. A. H. Luttik, J. P. van Dijken, J. T. Pronk, P. Klaassen, H. F. M. Boelens, R. J. T. de Mattos, K. van Dam, and A. L. Kruckeberg. 1999. Glucose uptake kinetics and transcription of HXT genes in chemostat cultures of Saccharomyces cerevisiae. J. Biol. Chem. 274:15350-15359.
11. Dietvorst, J., J. Londesborough, and H. Y. Steensma. 2005. Maltotriose utilization in lager yeast strains: MTT1 encodes a maltotriose transporter. Yeast 22:775-788.
12. Domingues, L., J. A. Teixeira, and N. Lima. 1999. Construction of a flocculent Saccharomyces cerevisiae fermenting lactose. Appl. Microbiol. Biotechnol. 51:621-626.
13. Eisenthal, R., and A. Cornish-Bowden. 1974. The direct linear plot. A new graphical procedure for estimating enzyme kinetic parameters. Biochem. J. 139:715-720.
14. Guimarães, P. M. R., H. Virtanen, and J. Londesborough. 2006. Direct evidence that maltose transport activity is affected by the lipid composition of brewer's yeast. J. Inst. Brew. 112:203-209.
15. Guimarães, P. M. R., J. François, J. L. Parrou, J. A. Teixeira, and L. Domingues. 2008. Adaptive evolution of a lactose-consuming Saccharomyces cerevisiae recombinant. Appl. Environ. Microbiol. 74:1748-1756.
16. Guimarães, P. M. R., and J. Londesborough. 2008. The adenylate energy charge and specific fermentation rate of brewer's yeasts fermenting high- and very high-gravity worts. Yeast 25:47-58.
17. Han, E. K., F. Cotty, C. Sottas, H. Jiang, and C. A. Michels. 1995. Characterization of AGT1 encoding a general α-glucoside transporter from Saccharomyces. Mol. Microbiol. 17:1093-1107.
18. Hauer, R., and M. Hofer. 1978. Evidence for interactions between the energy-dependent transport of sugars and the membrane potential in the yeast Rhodotorula gracilis (Rhodosporidium toruloides). J. Membr. Biol. 43:335-349.
19. Jespersen, L., L. B. Cesar, P. G. Meaden, and M. Jakobsen. 1999. Multiple α-glucoside transporter genes in brewer's yeast. Appl. Environ. Microbiol. 65:450-456.
20. Kim, S. H., K. P. Lim, and H. S. Kim. 1997. Differences in the hydrolysis of lactose and other substrates by β-D-galactosidase from Kluyveromyces lactis. J. Dairy Sci. 80:2264-2269.
21. Kodama, Y., N. Fukui, T. Ashikari, Y. Shibano, K. Morioka-Fujimoto, Y. Hiraki, and K. Nakatani. 1995. Improvement of maltose fermentation efficiency: constitutive expression of MAL genes in brewing yeasts. J. Am. Soc. Brew. Chem. 53:24-29.
22. Lages, F., and C. Lucas. 1997. Contribution to the physiological characterization of glycerol active uptake in Saccharomyces cerevisiae. Biochim. Biophys. Acta 1322:8-18.
23. Lagunas, R. 1993. Sugar transport in Saccharomyces cerevisiae. FEMS Microbiol. Rev. 104:229-242.
24. Lillie, S. H., and J. R. Pringle. 1980. Reserve carbohydrate metabolism in Saccharomyces cerevisiae: responses to nutrient limitation. J. Bacteriol. 143:1384-1394.
25. Lowry, O. H., N. J. Rosebrough, A. L. Farr, and R. J. Randall. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193:265-275.
26. Lucero, P., M. Herweijer, and R. Lagunas. 1993. Catabolite inactivation of the yeast maltose transporter is due to proteolysis. FEBS Lett. 333:165-168.
27. Lucero, P., É. Peñalver, E. Moreno, and R. Lagunas. 1997. Moderate concentrations of ethanol inhibit endocytosis of the yeast maltose transporter. Appl. Environ. Microbiol. 63:3831-3836.
28. Lucero, P., E. Moreno, and R. Lagunas. 2002. Catabolite inactivation of the sugar transporters in Saccharomyces cerevisiae is inhibited by the presence of a nitrogen source. FEMS Yeast Res. 1:307-314.
29. Lundin, A. 2000. Use of firefly luciferase in ATP-related assays of biomass, enzymes and metabolites. Methods Enzymol. 305:346-370.
30. Medintz, I., H. Jiang, E. K. Han, W. Cui, and C. A. Michels. 1996. Characterization of the glucose-induced inactivation of maltose permease in Saccharomyces cerevisiae. J. Bacteriol. 178:2245-2254.
31. Miller, G. L. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
32. Nobre, A., C. Lucas, and C. Leão. 1999. Transport and utilization of hexoses and pentoses in the halotolerant yeast Debaryomyces hansenii. Appl. Environ. Microbiol. 65:3594-3598.
33. Numanoglu, Y., and S. Sungur. 2004. β-Galactosidase from Kluyveromyces lactis cell disruption and enzyme immobilization using a cellulose-gelatin carrier system. Process Biochem. 39:703-709.
34. Perlman, D., P. Raney, and H. O. Halvorson. 1984. Cytoplasmic and secreted Saccharomyces cerevisiae invertase mRNAs encoded by one gene can be differentially or coordinately regulated. Mol. Cell. Biol. 4:1682-1688.
35. Rautio, J., and J. Londesborough. 2003. Maltose transport by brewer's yeasts in brewer's wort. J. Inst. Brew. 109:251-261.
36. Rubio-Texeira, M. 2005. A comparative analysis of the GAL genetic switch between not-so-distant cousins: Saccharomyces cerevisiae versus Kluyveromyces lactis. FEMS Yeast Res. 5:1115-1128.
37. Salema-Oom, M., V. V. Pinto, P. Gonçalves, and I. Spencer-Martins. 2005. Maltotriose utilization by industrial Saccharomyces strains: characterization of a new member of the α-glucosidc transporter family. Appl. Environ. Microbiol. 71:5044-5049.
38. Schwencke, J., H. Canut, and A. Flores. 1983. Simultaneous isolation of the yeast cytosol and well-preserved mitochondria with negligible contamination by vacuolar proteases. FEBS Lett. 156:274-280.
39. Serrano, R. 1977. Energy requirements for maltose transport in yeast. Eur. J. Biochem. 80:97-102.
40. Serrano, R. 1991. Transport across yeast vacuolar and plasma membranes. In E. W. Jones, J. R. Pringle, and J. R. Broach (ed.), The molecular and cellular biology of the yeast Saccharomyces: genome dynamics, protein synthesis and energetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
41. Sheetz, R. M., and R. C. Dickson. 1980. Mutations affecting synthesis of β-galactosidase activity in the yeast Kluyveromyces lactis. Genetics 95:877-890.
42. Slayman, C. L., P. Kaminski, and D. Stetson. 1989. Structure and function of fungal plasma membrane ATPases. In P. J. Kuhn, A. P. J. Princi, M. J. Jung, M. W. Goosey, and L. G. Copping (ed.), Biochemistry of cell walls and membranes in fungi. Springer Verlag KG, Berlin, Germany.
43. Stambuk, B. U., M. A. da Silva, A. D. Panek, and P. S. de Araujo. 1999. Active α-glucoside transport in Saccharomyces cerevisiae. FEMS Microbiol. Lett. 170:105-110.
44. +/methyl β-D-thiogalactoside symport in Saccharomyces fragilis. Biochim. Biophys. Acta 693:213-220.
45. +-galactoside symport in the yeast Kluyveromyces marxianus. Biochem. J. 242:729-734.
46. van der Rest, M. E., A. H. Kamminga, A. Nakano, Y. Anraku, B. Poolman, and W. N. Konings. 1995. The plasma membrane of Saccharomyces cerevisiae: structure, function and biogenesis. Microbiol. Rev. 59:304-322.
47. Verduyn, C., E. Postma, W. A. Scheffers, and J. P. van Dijken. 1992. Effect of benzoic acid on metabolic fluxes in yeasts: a continuous-culture study on the regulation of respiration and alcoholic fermentation. Yeast 8:501-517.
48. Walsh, M. C., H. P. Smits, M. Scholte, and K. van Dam. 1994. Affinity of glucose transport in Saccharomyces cerevisiae is modulated during growth on glucose. J. Bacteriol. 176:953-958.
49. Walsh, M. C., H. P. Smits, and K. van Dam. 1994. Respiratory inhibitors affect incorporation of glucose into Saccharomyces cerevisiae cells but not the activity of glucose transport. Yeast 10:1553-1558.
50. Weusthuis, R. A., H. Adams, W. A. Scheffers, and J. P. van Dijken. 1993. Energetics and kinetics of maltose transport in Saccharomyces cerevisiae: a continuous culture study. Appl. Environ. Microbiol. 59:3102-3109.